Literature DB >> 31310802

Differential toxicity of ataxin-3 isoforms in Drosophila models of Spinocerebellar Ataxia Type 3.

Sean L Johnson1, Jessica R Blount1, Kozeta Libohova1, Bedri Ranxhi1, Henry L Paulson2, Wei-Ling Tsou3, Sokol V Todi4.   

Abstract

The most commonly inherited dominant ataxia, Spinocerebellar Ataxia Type 3 (SCA3), is caused by a CAG repeat expansion that encodes an abnormally long polyglutamine (polyQ) repeat in the disease protein ataxin-3, a deubiquitinase. Two major full-length isoforms of ataxin-3 exist, both of which contain the same N-terminal portion and polyQ repeat, but differ in their C-termini; one (denoted here as isoform 1) contains a motif that binds ataxin-3's substrate, ubiquitin, whereas the other (denoted here as isoform 2) has a hydrophobic tail. Most SCA3 studies have focused on isoform 1, the predominant version in mammalian brain, yet both isoforms are present in brain and a better understanding of their relative pathogenicity in vivo is needed. We took advantage of the fruit fly, Drosophila melanogaster to model SCA3 and to examine the toxicity of each ataxin-3 isoform. Our assays reveal isoform 1 to be markedly more toxic than isoform 2 in all fly tissues. Reduced toxicity from isoform 2 is due to much lower protein levels as a result of its expedited degradation. Additional studies indicate that isoform 1 is more aggregation-prone than isoform 2 and that the C-terminus of isoform 2 is critical for its enhanced proteasomal degradation. According to our results, although both full-length, pathogenic ataxin-3 isoforms are toxic, isoform 1 is likely the primary contributor to SCA3 due to its presence at higher levels. Isoform 2, as a result of rapid degradation that is dictated by its tail, is unlikely to be a key player in this disease. Our findings provide new insight into the biology of this ataxia and the cellular processing of the underlying disease protein.
Copyright © 2019 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Ataxia; Drosophila; Isoform; Neurodegeneration; Polyglutamine; Proteasome

Mesh:

Substances:

Year:  2019        PMID: 31310802      PMCID: PMC6834911          DOI: 10.1016/j.nbd.2019.104535

Source DB:  PubMed          Journal:  Neurobiol Dis        ISSN: 0969-9961            Impact factor:   5.996


  75 in total

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Authors:  Carlos A Matos; Sandra de Macedo-Ribeiro; Ana Luísa Carvalho
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3.  CAG repeats containing CAA interruptions form branched hairpin structures in spinocerebellar ataxia type 2 transcripts.

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4.  Increased transcript diversity: novel splicing variants of Machado-Joseph disease gene (ATXN3).

Authors:  Conceição Bettencourt; Cristina Santos; Rafael Montiel; Maria do Carmo Costa; Pablo Cruz-Morales; Liliana Ribeiro Santos; Nelson Simões; Teresa Kay; João Vasconcelos; Patrícia Maciel; Manuela Lima
Journal:  Neurogenetics       Date:  2009-08-28       Impact factor: 2.660

5.  RNA structure of trinucleotide repeats associated with human neurological diseases.

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Journal:  Nucleic Acids Res       Date:  2003-10-01       Impact factor: 16.971

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Authors:  Amy C Groth; Matthew Fish; Roel Nusse; Michele P Calos
Journal:  Genetics       Date:  2004-04       Impact factor: 4.562

Review 7.  Polyglutamine Repeats in Neurodegenerative Diseases.

Authors:  Andrew P Lieberman; Vikram G Shakkottai; Roger L Albin
Journal:  Annu Rev Pathol       Date:  2018-08-08       Impact factor: 23.472

8.  Nuclear localization of ataxin-3 is required for the manifestation of symptoms in SCA3: in vivo evidence.

Authors:  Ulrike Bichelmeier; Thorsten Schmidt; Jeannette Hübener; Jana Boy; Lukas Rüttiger; Karina Häbig; Sven Poths; Michael Bonin; Marlies Knipper; Werner J Schmidt; Johannes Wilbertz; Hartwig Wolburg; Franco Laccone; Olaf Riess
Journal:  J Neurosci       Date:  2007-07-11       Impact factor: 6.167

9.  DnaJ-1 and karyopherin α3 suppress degeneration in a new Drosophila model of Spinocerebellar Ataxia Type 6.

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Journal:  Hum Mol Genet       Date:  2015-05-07       Impact factor: 6.150

10.  Mouse ataxin-3 functional knock-out model.

Authors:  Pawel M Switonski; Agnieszka Fiszer; Katarzyna Kazmierska; Maciej Kurpisz; Wlodzimierz J Krzyzosiak; Maciej Figiel
Journal:  Neuromolecular Med       Date:  2010-10-14       Impact factor: 3.843

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  11 in total

Review 1.  The Drosophila melanogaster as Genetic Model System to Dissect the Mechanisms of Disease that Lead to Neurodegeneration in Adrenoleukodystrophy.

Authors:  Margret H Bülow; Brendon D Parsons; Francesca Di Cara
Journal:  Adv Exp Med Biol       Date:  2020       Impact factor: 2.622

2.  Consensus Paper: Strengths and Weaknesses of Animal Models of Spinocerebellar Ataxias and Their Clinical Implications.

Authors:  Jan Cendelin; Marija Cvetanovic; Mandi Gandelman; Hirokazu Hirai; Harry T Orr; Stefan M Pulst; Michael Strupp; Filip Tichanek; Jan Tuma; Mario Manto
Journal:  Cerebellum       Date:  2021-08-10       Impact factor: 3.648

Review 3.  Mutant Ataxin-3-Containing Aggregates (MATAGGs) in Spinocerebellar Ataxia Type 3: Dynamics of the Disorder.

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Journal:  Mol Neurobiol       Date:  2021-02-24       Impact factor: 5.590

4.  Isoleucine 44 Hydrophobic Patch Controls Toxicity of Unanchored, Linear Ubiquitin Chains through NF-κB Signaling.

Authors:  Jessica R Blount; Kozeta Libohova; Gustavo M Silva; Sokol V Todi
Journal:  Cells       Date:  2020-06-22       Impact factor: 6.600

5.  Endurance exercise ameliorates phenotypes in Drosophila models of spinocerebellar ataxias.

Authors:  Alyson Sujkowski; Kristin Richardson; Matthew V Prifti; Robert J Wessells; Sokol V Todi
Journal:  Elife       Date:  2022-02-16       Impact factor: 8.140

6.  Drosophila as a Model of Unconventional Translation in Spinocerebellar Ataxia Type 3.

Authors:  Sean L Johnson; Matthew V Prifti; Alyson Sujkowski; Kozeta Libohova; Jessica R Blount; Luke Hong; Wei-Ling Tsou; Sokol V Todi
Journal:  Cells       Date:  2022-04-04       Impact factor: 6.600

7.  Degron capability of the hydrophobic C-terminus of the polyglutamine disease protein, ataxin-3.

Authors:  Jessica R Blount; Sean L Johnson; Kozeta Libohova; Sokol V Todi; Wei-Ling Tsou
Journal:  J Neurosci Res       Date:  2020-07-09       Impact factor: 4.164

8.  Sylvian fissure development is linked to differential genetic expression in the pre-folded brain.

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9.  Ubiquitin-interacting motifs of ataxin-3 regulate its polyglutamine toxicity through Hsc70-4-dependent aggregation.

Authors:  Sean L Johnson; Bedri Ranxhi; Kozeta Libohova; Wei-Ling Tsou; Sokol V Todi
Journal:  Elife       Date:  2020-09-21       Impact factor: 8.140

10.  Targeting the VCP-binding motif of ataxin-3 improves phenotypes in Drosophila models of Spinocerebellar Ataxia Type 3.

Authors:  Sean L Johnson; Kozeta Libohova; Jessica R Blount; Alyson L Sujkowski; Matthew V Prifti; Wei-Ling Tsou; Sokol V Todi
Journal:  Neurobiol Dis       Date:  2021-09-24       Impact factor: 5.996

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